Abstract
We present new insights into the phylogeography of the Robin, Erithacus rubecula, from the seven Azores Islands where it breeds, based on sequences of mitochondrial and nuclear genes from 35 individuals (five from each of the seven islands) as well as outgroup/comparison samples from Madeira, Canary Islands and Continental Western Palearctic (Europe and North Africa). To understand the level of concordance between the genetic data and morphometric variability, eight morphometric characters were analysed for 113 birds for the seven Azores Islands populations. Our results revealed that Robins from the Azores possess low genetic diversity and share their most common haplotype with Madeira and the Continental Western Palearctic Robins, which support the hypothesis of one recent founder event and a fast range expansion to most of the Azores Islands. Nevertheless, despite this lack of neutral genetic differentiation, morphological differences were found among islands, which could be attributed to natural selection processes. The morphological data show that birds from São Miguel had the longest wings and largest body mass, and that birds from Graciosa had the smallest bill length. This recent colonisation could be the reason for the absence of Robins in the westernmost islands of the Azores.
Zusammenfassung
Phylogeographie und genetische Diversität des Rotkehlchens ( Erithacus rubecula ) auf den Azoren: Hinweise auf eine kürzlich erfolgte Besiedlung
Wir stellen neue Erkenntnisse zur Phylogeographie des Rotkehlchens (Erithacus rubecula) auf den sieben Azoreninseln, auf denen es brütet, vor, die auf den Sequenzen mitochondrialer und nukleärer Gene von 35 Individuen (fünf von jeder Insel) sowie Außengruppen-/Vergleichsproben aus Madeira, den Kanaren und der kontinentalen westlichen Paläarktis (Europa und Nordafrika) basieren. Um das Ausmaß der Übereinstimmung zwischen den genetischen Daten und der morphometrischen Variabilität zu verstehen, haben wir acht morphometrische Merkmale für 113 Vögel aus den sieben Azoreninselpopulationen analysiert. Unsere Ergebnisse zeigten, dass Rotkehlchen von den Azoren eine niedrige genetische Diversität aufweisen und den häufigsten Haplotyp mit den Rotkehlchen aus Madeira und der kontinentalen westlichen Paläarktis teilen, was die Hypothese eines kürzlich erfolgten Besiedlungsereignisses und einer schnellen Ausweitung des Verbreitungsgebiets auf die meisten Azoreninseln stützt. Trotz dieses Mangels an neutraler genetischer Differenzierung wurden morphometrische Unterschiede zwischen den Inseln gefunden, die auf natürliche Selektionsprozesse zurückgeführt werden konnten. Die morphologischen Daten zeigen, dass Vögel aus São Miguel die längsten Flügel sowie die größte Körpermasse und Vögel aus Graciosa die kürzesten Schnäbel aufwiesen. Diese erst kürzlich erfolgte Besiedlung könnte der Grund dafür sein, dass Rotkehlchen auf den westlichsten Azoreninseln fehlen.
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References
Arctander P, Folmer O, Fjeldsa J (1996) The phylogenetic relationships of Berthelot’s pipit Anthus berthelotti illustrated by DNA sequence data, with remarks on the genetic distance between Rock and Water pipits Anthus spinoletta. Ibis 138:263–272
Bannerman DA, Bannerman WN (1966) Birds of the Atlantic Islands. vol. 3: a history of the birds of the Azores. Oliver and Boyd, Edinburgh
Barton NH, Charlesworth B (1984) Genetic revolutions, founder effects, and speciation. Annu Rev Ecol Sys 15:133–164
Barton NH, Mallet J (1996) Natural selection and random genetic drift as causes of evolution on islands (and discussion). Phil Trans R Soc B 351:785–795
Bergmann H, Schottler B (2001) Tenerife Robin—a species of its own? Dutch Birding 23:140–146
Brown WM, George MJR, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 74:1967–1971
Clarke T, Orgill C, Disley T (2006) Field guide to the birds of the Atlantic Islands: Canary Islands, Madeira, Azores. Helm Field Guides, Cape Verde
Clegg SM, Phillimore A (2010) The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu. Phil Trans R Soc B 365:1077–1092
Clegg SM, Degnan CM, Estoup A, Kikkawa J, Owens IPF (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–2099
Clement M, Posada D, Crandall KA (2000) TCS: a computer programme to estimate gene genealogies. Mol Ecol 9:1657–1660
Clements JF (2000) Birds of the World. A checklist. Pica Press, Sussex
Cramp S (1988) Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic. vol 5: Tyrant flycatchers to thrushes. Oxford University Press, Oxford, UK
del Hoyo J, Elliott A, Christie D (2006) Handbook of the birds of the world. Vol. 11: old world Flycatchers to old world warblers. Lynx Editions, Barcelona, Spain
Dietzen C, With HH, Wink M (2003) The phylogeographic differentiation of the European Robin Erithacus rubecula on the Canary Islands revealed by mitochondrial DNA sequence data and morphometrics: evidence for a new Robin taxon on Gran Canaria? Avian Sci 3:115–131
Dietzen C, Voigt C, Wink M, Gahr M, Leitner S (2006) Phylogeography of island canary (Serinus canaria) populations. J Ornithol 147:485–494
Equipa Atlas (2008) Atlas das Aves Nidificantes em Portugal (1999–2005). Instituto da Conservação da Natureza e da Biodiversidade, Sociedade Portuguesa para o Estudo das Aves, Parque Natural da Madeira e Secretaria Regional do Ambiente e do Mar. Assírio & Alvim, Lisboa, Portugal
França Z, Cruz JV, Nunes JC, Forjaz VH (2003) Geologia dos Açores: uma perspectiva actual. Açoreana 10:11–140
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Fu YX, Li WH (1993) Statistical test of neutrality of mutations. Genetics 133:693–709
Grant P, Grant R (2008) How and why species multiply. The radiation of Darwin’s finches. Princeton University Press, New Jersey
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Hartert JC, Olgivie-Grant WR (1905) On the birds of the Azores. Novi Zool 12:80–128
Helbig AJ, Martens J, Henning F, Schottler B, Seibold I, Wink M (1996) Phylogeny and species limits in the Palaearctic Chiffchaff Phylloscopus collybita complex: mitochondrial genetic differentiation and bioacoustic evidence. Ibis 138:650–666
Hounsome MC (1993) Biometrics and origins of some Atlantic island birds. Bol Mus Mun Funchal 2:107–129
Illera JC, Koivula K, Broggi J, Päckert M, Martens J, Kvist L (2011) A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group. Mol Ecol 20:4123–4139
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Marshall HD, Baker AJ (1999) Colonisation History of Atlantic Island Common Chaffinches (Fringilla coelebs) Revealed by Mitochondrial DNA. Mol Phylogenet Evol 11:201–212
Martin A, Lorenzo JA (2001) Aves del Archipélago Canario. Francisco Lemus, Editor SL. La Laguna, Tenerife
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Neves VC, Griffiths K, Savory FR, Furness RW, Mable BK (2010) Are European starlings breeding in the Azores archipelago genetically distinct from birds breeding in mainland Europe? Eur J Wild Res 59:95–100
Päckert M, Martens J (2004) Song dialects on the Atlantic islands: goldcrests of the Azores (Regulus regulus azoricus, R. r. sanctae-mariae, R. r. inermis). J Ornithol 145:23–30
Päckert M, Dietzen C, Martens J, Wink M, Kvist L (2006) Radiation of Atlantic Goldcrests Regulus regulus spp.: evidence of a new taxon from the Canary Islands. J Avian Biol 37:364–380
Peck DR, Congdon BC (2004) Reconciling historical biogeography of the Catharus thrushes: a molecular phylogenetic approach. Auk 120:299–310
Pérez-Tris J, Carbonell R, Tellería JL (2000) Abundance distribution, morphological variation and juvenile condition of Robins, Erithacus rubecula (L.), in their Mediterranean range boundary. J Biogeogr 27:879–888
Petren K, Grant PR, Grant BR, Keller LF (2005) Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Mol Ecol 14:2943–2957
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality test against population growth. Mol Biol Evol 19:2092–2100
Rodrigues P, Bried J, Rodebrand S, Cunha R (2010) AVES. In: Borges PAV, Costa A, Cunha R, Gabriel R, Gonçalves V, Martins AF, Melo I, Parente M, Raposeiro P, Rodrigues P, Santos RS, Silva L, Vieira P, Vieira V (eds) A list of the terrestrial and marine biota from the Azores. Princípia, Cascais
Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615
Samarasin-Dissanayake P (2010) Population differentiation, historical demography and evolutionary relationships among widespread Common Chaffinch populations (Fringilla coelebs ssp.). Thesis for the degree of Master of Science, University of Toronto
Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. User manual ver 2.000. Genetics and Biometry Laboratory Department of Anthropology, University of Geneva, Geneva, Italy
StatSoft Inc (2007) STATISTICA (data analysis software system), version 8.0. www.statsoft.com
Steeves TE, Anderson DJ, Friesen VL (2005) The isthmus of Panama: a major physical barrier to gene flow in a highly mobile pantropical seabird. J Evol Biol 18:1000–1008
Suárez NM, Betancor E, Klassert TE, Almeida T, Hernández M, Pestano JJ (2009) Phylogeography and genetic structure of the Canarian common Chaffinch (Fringilla coelebs) inferred with mtDNA and microsatellite loci. Mol Phylogenet Evol 53:556–564
Svensson L (1992) Identification guide to European Passerines. L. Svensson, Stockholm
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465
Thompson B (1991) Methods, plainly speaking: a primer on the logic and use of canonical correlation analysis. Mes Eval Couns Dev 24:80–93
von Haeseler A, Sajantila A, Paabo S (1996) The genetical archaeology of the human genome. Nat Genet 14:135–140
Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328
Wink M, Sauer-Gürth H, Gwinner E (2002) Evolutionary relationships of stonechats and related species inferred from mitochondrial-DNA sequences and genomic fingerprinting. Brit Birds 95:349–355
Wittmann U, Heidrich P, Wink M, Gwinner E (1995) Speciation in the stonechat Saxicola torquata inferred from nucleotide sequences of the cytochrome-b gene. J Zoo Syst Evol Res 33:116–122
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, New Jersey
Acknowledgments
We would like to thank the Direção Regional do Ambiente dos Açores for their kind permission to capture birds and collect blood samples from the Azores (permission 119/2011/DRA). To Parque Natural da Madeira for the permission to take samples from Madeira (permission 01–A/2011/FAU/MAD). To Instituto da Conservação da Natureza e da Biodiversidade for the ring permission (152/2011). To Jan Lifjeld and the National Centre for Biosystematics team of the Natural History Museum of Oslo for their support during the field trip to Madeira. To Joana Micael and Roberto Resendes for their support in the field; to Paulo Tenreiro for collecting samples from Portugal; and to André Eloy, Associação de Juventude da ilha Graciosa, Atlânticoline, Bárbara Gravanita, Grupo Bensaude, EDA, Even Stensrud, Fernando Cunha, João Melo, José Marcelino, Pedro Domingues and Robin Kersten for their support along the Azores Islands. To Nicolle Mode and Therese Catanach for the English revision of this manuscript. P Rodrigues and RJ Lopes were supported by grant funding from FCT - Portuguese Foundation for Science and Technology (SFRH/BD/36084/2007 and SFRH/BPD/40786/2007 respectively). The study was also partially supported by FCT project PTDC/BIA-BEC/103435/2008 to S. Drovetski. All the conducted experiments comply with the current laws of Portugal and the authors declare that they have no conflict of interest.
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Rodrigues, P., Lopes, R.J., Drovetski, S.V. et al. Phylogeography and genetic diversity of the Robin (Erithacus rubecula) in the Azores Islands: Evidence of a recent colonisation. J Ornithol 154, 889–900 (2013). https://doi.org/10.1007/s10336-013-0953-4
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DOI: https://doi.org/10.1007/s10336-013-0953-4